Meat Science 92 (2012) 290–296

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Meat Science

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Review Innovations in value-addition of edible meat by-products

Fidel Toldrá a,⁎, M.-Concepción Aristoy a, Leticia Mora a, Milagro Reig b a Instituto de Agroquímica y Tecnología de Alimentos (CSIC), Avenue Agustín Escardino 7, 46980 Paterna (Valencia), Spain b Instituto de Ingeniería de Alimentos para el Desarrollo, Universidad Politécnica de Valencia, Camino de Vera s/n, 46022 Valencia, Spain article info abstract

Keywords: While muscle foods are the more commonly consumed portion of an animal, meat by-products such as the Animal by-products entrails and internal organs are also widely consumed. Considered high-priced delicacies or waste material Meat by-products to be tossed away, the use and value of offal-edible and inedible meat by-products depend entirely on the Functional substances culture and country in question. The skin, blood, bones, meat trimmings, fatty tissues, horns, hoofs, feet, Bioactive peptides skull, and internal organs of harvested animals comprise a wide variety of products including human or Antimicrobial peptides pet food or processed materials in animal feed, fertilizer, or fuel. Industry is using science and innovation Hydrolyzed proteins fi fi Value-added to add value to animal by-products far beyond its usual pro tability. Regardless of the nal product's desti- nation, it is still necessary to employ the most up-to-date and effective tools to analyze these products for nu- tritional properties, to search for key active molecules in nutrition like bioactive peptides, food safety (antimicrobial peptides), medicine, cosmetics or other fields, to develop new technological applications and to continue innovation towards advanced value-addition of meat by-products. © 2012 Elsevier Ltd. All rights reserved.

Contents

1. Introduction ...... 290 2. Safety issues ...... 291 3. Edible meat by-products as human food ...... 291 3.1. Blood and blood products...... 292 3.2. Proteins: generation of bioactive peptides ...... 292 3.3. Protein: generation of antimicrobial peptides ...... 294 3.4. Proteins: other food applications ...... 294 4. Feed and pet food applications...... 294 5. Other non-food, non-feed industrial applications ...... 294 6. Conclusions ...... 295 Acknowledgments ...... 295 References ...... 295

1. Introduction reduce by-products but there is a growing awareness that most times these by-products are under-utilized and represent a valuable Slaughterhouses as well as the processing of meats generate a sig- resource if treated in the correct manner. nificant amount of solid and liquid by-products. Wholesalers, retailers It is no longer practical to discard by-products and wastes, espe- and renderers also produce large amounts of by-products. So, millions cially when a significant amount of valuable raw materials have a of tons of processing wastes are produced every day and the problem strong economic potential like the production of new products and is the disposal of such wastes, which remains a huge problem for the functional ingredients with a significant added-value (Toldrá & Reig, processors. The disposal of processing by-products and wastes incurs 2011; Zhang, Xiao, Samaraweera, Lee, & Ahn, 2010). It is desirable considerable cost to processors for their treatment according to strict to process all by-products into valuable products, for human foods, regulations. Of course, there are industrial systems to treat and pet foods, animal feeds, pharmaceuticals, or fertilizer and lately for biodiesel generation. New technologies and uses for meat by- ⁎ Corresponding author. Tel.: +34 963900022; fax: +34 963636301. products have been developed around the world but most times E-mail address: [email protected] (F. Toldrá). they are difficult to be implemented. The reason is the difficulties

0309-1740/$ – see front matter © 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2012.04.004 F. Toldrá et al. / Meat Science 92 (2012) 290–296 291 found to combine the use of innovative technology, processing in 1982 in UK. It affects adult cattle; BSE has not been detected in an- methods, and adequate marketing of the product. imals younger than 30 months. BSE belongs to a family of diseases Adding value to meat by-products implies a degree of innovation known as transmissible spongiform encephalopathies (TSEs), which that makes a by-product that could be considered as waste, to be result from the build-up of abnormal prion proteins in the brain and used as raw material subjected to further processing into edible central nervous system. A TSE disease that affects humans is the Var- food items desirable to consumers (Ockerman & Basu, 2004a) or in- iant Creuzfeldt–Jacob Disease (vCJD) which causes death. Because of edible products with economic profitability (e.g. plastics, pharmaceu- this disease, certain tissues of cattle (spleen, tonsils, intestine, mesen- ticals, energy) (Ockerman & Basu, 2004b; Pearl, 2004). In the case of tery, spinal cord and full head), sheep and goats (full head, ileum, edible items, meat by-products constitute an excellent source of nu- spleen and spinal cord if a permanent incisor tooth erupted through trients like essential amino acids, minerals and vitamins (Aristoy & the gums or are aged over 12 months) that are most likely to contain Toldrá, 2011; García-Llatas, Alegría, Barberá, & Farré, 2011; Honikel, the BSE agent are considered to be specified risk materials and they 2011; Kim, 2011). Such added value can be obtained in terms of must be removed and destroyed in order to avoid their inclusion in shelf stability, improved technological functions (flavoring com- either the human or animal food chains. In countries with risk of pounds, water bonding agents, emulsifiers), better sensory quality BSE, the bones from beef, sheep and goats are also considered to be (color, texture, flavor) or even more convenience. Another alternative specified risk materials and they are also forbidden for the production is to produce functional ingredients like bioactive peptides and anti- of mechanically recovered meat. Sheep and goats may suffer from oxidants. A good example is blood that has a long history of use in scrapie which is another TSE disease that, even though not affecting Europe and Asia as an ingredient in traditional foods like blood humans, may mask BSE detection. In the European Union, the rules sausages, puddings, blood soups and crackers. Blood serves several for the prevention, control and eradication of certain transmissible technological functions such as the increase in protein levels, and spongiform encephalopathies are described in Regulation 999/2001 the enhancement of the water binding and emulsification capacity (EC, 2001). Regulation 853/2004 (EC, 2004) describes the specific (Mandal, Rao, Kowale, & Pal, 1999; Ofori & Hsieh, 2011). On the con- hygiene rules for foodstuffs including those of animal origin while trary, blood products use to be discarded in the USA as an unwanted health rules regarding animal by-products and derived products not by-product; for instance, beef plasma is no longer used in the United intended for human consumption and repealing the animal by- States for surimi or other food preparations. products Regulation (EC) No 1774/2002 are described in Regulation Meat industry is using science and innovation to add value to an- 1069/2009 (EC, 2009). The Food and Drug Administration (FDA, imal by-products far beyond its usual profitability based on hides and 2004) also announced new rules to prevent the establishment and internal organs. Appropriate research and development activity can spread of bovine spongiform encephalopathy (BSE) in the United help to convert animal by-products into key components (bioactive States, including a prohibition on the use of high-risk, cattle-derived molecules) in scientific, medical, and technological advances. In sum- materials that can carry the BSE agent which are defined as specified mary, the processing of by-products can convert a product of low risk material. These materials are brain, skull, eyes, trigeminal ganglia, value, or even having relevant disposal costs, into a product capable spinal cord, vertebral column and the dorsal root ganglia of cattle of covering all the processing and disposal costs, and reducing the en- more than 30 months of age and also the tonsils and the distal vironmental damage. A diagram showing the main routes for applica- ileum of the small intestine of cattle of any age. The small intestine tions of meat by-products is shown in Fig. 1. This manuscript reviews of all cattle, and mechanically separated meat from beef are also the latest innovations to add value to edible meat by-products far banned. beyond its usual profitability. 3. Edible meat by-products as human food 2. Safety issues The consideration of by-product depends on the market demand. So, Apart from strict hygiene considerations, there are other recent is- some non-carcass products that are considered inedible in a country sues that deserve attention when treating meat by-products. Bovine can be considered as precious products in other countries (Ockerman spongiform encephalopathy (BSE) is a disease that was first detected & Basu, 2004a; Spoonger, 1988). By-products such as blood, liver,

Slaughterhouse Meat processing

Blood Hair nails Hydrolysis Trimmings Bones MRM DBP Plasma RBC Globin Rendering Heme Fat Thrombin+ Functional Iron Feed Fibrinogen agents peptide

Protein Cosmetics Lard hydrolysate Chemicals Tallow Hydrolysis

Biodiesel Protein Antimicrobial Functional hydrolysate peptides peptides

Fig. 1. Flow diagram of main routes for value-addition to meat by-products. 292 F. Toldrá et al. / Meat Science 92 (2012) 290–296 lung, heart, kidney, brains, spleen and tripe have good nutritive value feed ingredients due to their good gelation and emulsification properties (Anderson, 1988; Honikel, 2011) and constitute part of the diet in dif- (Cofrades, Guerra, Carballo, Fernández-Martin, & Jiménez-Colmenero, ferent countries worldwide (Nollet & Toldrá, 2011). For instance, liver 2000). Some of the plasma proteins have shown good cross-linking ability is very rich in vitamins (Kim, 2011) while liver and kidney contain a of major proteins and protease inhibitory activity (Kang & Lanier, 1999) wide variety of minerals and trace elements (García-Llatas et al., or used to enrich in protein products like pasta (Yousif, Cranston, & 2011) even though cholesterol content is quite high (Bragagnolo, Deeth, 2003). Other precipitated blood plasma compounds like fibrinogen 2011). Other products rich in fat tissue like lard or tallow contribute and the enzyme thrombin are used under the trade mark fibrimex® mostly to energy intake. It must be taken into account that the functions (Harimex, The Netherlands) as a binder for meat processing to manufac- and usefulness of some types of organs depend on the animal species ture restructured meat products. When both thrombin and fibrinogen from which they are obtained due to fluctuations in nutrients content. are mixed and applied to the surfaces of meat pieces, the thrombin en- For instance, vitamin A may vary from 50,000 RE μg for heart lamb, to zyme converts soluble fibrinogen into insoluble fibrin polymer giving 20,000 RE μg for pork heart or 18,000 RE μg for chicken heart rise to a half-staggered structure called the protofibril that finally aggre- (Honikel, 2011). gates to form fibers and yielding a three-dimensional network fibrin Some examples of typical consumption in certain countries of clot (Lennon, McDonald, Moon, Ward, & Kenny, 2010; Ryan, Mockros, meat trimmings, fatty tissues, horns, hoofs, feet, skull, and organs of Weisel, & Lorand, 1999). The resulting gel network gives meat emulsions harvested animals are briefly described in Table 1. In addition to typ- with modified physicochemical and textural characteristics, increasing ical uses in traditional foods, meat by-products have been the object the hardness and springiness (Herrero et al., 2007). The binding strength of innovative applications that are described below. depends on several factors like the pH and temperature of the meat, the moisture and in the case of restructured meat also the size of meat cuts 3.1. Blood and blood products (binding is stronger for larger particle size) and the direction of meat fibers (Boles & Shand, 1999; Chen & Lin, 2002). The hydrolysis of defi- Typical composition of bovine blood consists of 80.9% water, 17.3% brinated bovine plasma with either commercial enzymes like alcalase protein, 0.23% lipid, 0.07% carbohydrate, and 0.62% minerals (Duarte, or flavorzyme resulted in a mixture of peptides with molecular masses Carvalho Simoes, & Sgarbieri, 1999). Blood is mostly obtained from less than 6.50 kDa. The knowledge of the molecular weight distribution bovine and porcine sources and is made up of the cellular fraction is relevant in trying to predict the potential allergenicity, biological (red blood cells, white blood cells and platelets) and the plasma frac- activity, taste of the hydrolyzate and the types of volatile compounds tion (Ofori & Hsieh, 2011). generated during Maillard reaction (Wanasundara, Amarowicz, Pegg, & Blood proteins, especially those found in the plasma fraction, have rel- Shand, 2002). evant technological properties like gelation, foaming agents and emulsifi- There are not so many applications in the case of the cellular fraction cation that prompted the use of blood-derived products as value-added which is rich in red blood cells, probably due to the heme component of ingredients in the food industry and as dietary supplements (Ofori & hemoglobin that imparts a dark color and adverse flavor to the product Hsieh, 2011). For example, fractionated plasma proteins like immuno- (Duarte et al., 1999) or hygienic reasons (Ofori & Hsieh, 2011). It must globulins, fibrinogen and serum albumin, may be added to food and be remembered that despite hygienic precautions, the microbial con- tamination of blood may remain relatively high, making necessary the Table 1 application of preservation methods to minimize the total microbiota Examples of traditional consumption of different edible meat by-products. in the preserved blood (Toldrá et al., 2007). Adapted from Ockerman and Basu (2004a), Nollet and Toldrá (2011). The cellular fraction may be used in the meat industry as a color By-product Traditional consumption Examples of countries enhancer for sausages (Ofori & Hsieh, 2011). A better alternative to avoid sensory adverse effects is to remove hemoglobin to produce Liver Splinantero Greece, Turkey Sheep liver Iran globin or also known as decolorized blood that exhibits relevant tech- Paté All countries nological functions for replacing fat in meat products (Hsieh & Ofori, Almondega Portugal 2011; Viana, Silva, Delvivo, Bizzotto, & Silvestre, 2005). Faggots UK The enzymatic digestion of bovine hemoglobin produces heme Spleen Pani ca meusa (bread with spleen) Italy Heart Cooked and diced South America iron polypeptide which is commercialized for improving iron absorp- Kidney Kidney pie UK tion (Nissenson et al., 2003). An heme-iron enriched peptide product Brain Sesos South America, Spain was produced through a two stage enzymatic hydrolysis with com- Tongue Boiled or marinated South America mercial endo- and exo-peptidases to reach a high degree of hydroly- Ingredient in meat products Spain sis, within the range 30–40% (In, Chae, & Oh, 2002). The heme/ Testicles Criadillas Spain Tripe Blóomör, slátur Iceland peptide ratio increased with the molecular weight cut-off of the dial- Dinuguan Philippines ysis membrane reaching a ratio of 10% with ultrafiltration and diafil- Korouch Lebanon tration on a pilot scale. The obtained heme-enriched peptides were Callos Spain reported to contain higher iron content than hemoglobin constituting Cold appetizer China fi Haggis Scotland an interesting way to prepare heme-iron for the forti cation of com- Pieds et paquets France monly consumed foods and thus prevention of iron deficiency in Intestines Casings for sausages Mediterranean populations at risk. Blood Morcilla sausage Spain Different types of reactors have been designed to carry out blood Black pudding UK hemoglobin hydrolysis with simultaneous extraction of the hydroly- Thuringer blood sausage Germany fi Feet Pork's feet Spain zate. Membrane-ultra ltration reactors have been reported for such Khash Armenia purpose (Kapel et al., 2003; Vanhoute et al., 2010) and more recently, Ears Pork's ears Spain immobilized reactors with pepsin immobilized on a mineral support Khash Armenia like alumina (Ticu et al., 2005). Tail Rabo de toro (Bull's tail) Spain Tail pork Mediterranean Bones Gelatin soups Mediterranean 3.2. Proteins: generation of bioactive peptides Osso bucco Italy Lard, tallow Lard for cooking Northern Europe The proteolytic activity during meat processing generates a large Covering hams Mediterranean amount of peptides and free amino acids through proteolysis F. Toldrá et al. / Meat Science 92 (2012) 290–296 293

Meat by-products administration (Escudero, Sentandreu, Arihara, & Toldrá, 2010; Escudero, Sentandreu, & Toldrá, 2010; Escudero, 2012). Similar find- ings were reported for peptides generated from chicken breast pro- Extraction teins (Saiga et al., 2006) and a nonapeptide derived from porcine troponin C (Katayama et al., 2004). A few peptides with good in vitro and in vivo ACE-inhibitory activity against spontaneous hyper- tensive rats were reported from chicken collagen hydrolyzate Commercial Enzymatic reactor peptidases obtained with a protease from Aspergillus oryzae (Saiga et al., 2008). The thermolysin hydrolysis of pork meat proteins revealed two pentapeptides (Met-Asn-Pro-Pro-Lys and Ile-Thr-Thr-Asn-Pro) and Mixture of peptides six tripeptides (Met-Asn-Pro, Asn-Pro-Pro, Pro-Pro-Lys, Ile-Thr-Thr, Thr-Thr-Asn and Thr-Asn-Pro) with antihypertensive activity (Arihara, Nakashima, Mukai, Ishikawa, & Itoh, 2001). Similar peptides Fractionation and/or were obtained with thermolisin hydrolysis of myosin (Nakashima, Filtration/chromatography Arihara, Sasaki, Ishikawa, & Itoh, 2002). However, no in vivo activity results were provided so that there is a lack of evidence that these peptides would remain unaltered by digestive human proteases and Bioactive peptides extract be absorbed through the intestinal wall. A bovine gelatin hydrolyzate that was further hydrolyzed with Fig. 2. Flow diagram of the enzymatic hydrolysis of edible meat by-products for the thermolysin, was reported to show an intense in vitro angiotensin I- generation of bioactive peptides. converting enzyme inhibitory activity but also in vivo blood-pressure lowering effect in spontaneously rats. In fact, seven di and tripeptides (Ala-Gly, Ala-Gly-Pro, Val-Gly-Pro, Pro-Tyr, Gln-Tyr, Asp-Tyr and Ile- mechanisms (Toldrá, 2006). Endogenous muscle enzymes like cal- Tyr) were identified as being contributors to the antihypertensive effect pains and cathepsins in a first stage followed by the action of peptidyl- (Herregods et al., 2011). On the other hand, the gelatin hydrolyzate peptidases are responsible for such proteolysis (Arihara, 2006a; Mora without further thermolisin hydrolysis did not show any effect et al., 2009; Sentandreu & Toldrá, 2007). Apart from the endogenous (Herregods et al., 2011). generation, peptides can also be industrially obtained from meat pro- A number of bioactive peptides have been reported from peptic bo- tein wastes (trimmings, organs, collagen, hemoglobin) through vine hemoglobin hydrolyzates. Two potent peptides LGFPTTKTYFPHF hydrolysis with specific commercial proteases like papain, bromelain, and VVYPWT, corresponding respectively to the 34–46 fragment of thermolysine, pronase or proteinase K (Vercruysse, Van Camp, & the α chain and the 34–39 fragment of the β chain of porcine hemoglo- Smagghe, 2005). The enzymatic reaction can take place either in a bin, with in vitro inhibitory activity against the angiotensin converting batch-fed reactor or in a continuous way using an ultrafiltration enzyme (ACE) and having IC50 values of 4.92 and 6.02 μM, respectively, membrane reactor. The product is then submitted to fractionation were identified (Yu et al., 2006). These peptides are mostly located and partial purification either by filtration or chromatographic tech- around N- and C-terminal regions of α and β chains. However, no in niques (Arihara, 2006b). A scheme for such industrial production is vivo activity results have been provided and thus there is no evidence shown in Fig. 2. that these peptides might be absorbed intact or transported into the Hundreds of peptides are released but only a few, known as bioactive cell unaltered. peptides, are of interest because they are able to exert a determined Other bioactive hemoglobin-derived peptides include bradykinin- health benefit to the consumer through different types of bioactivity potentiating peptide (Lignot, Froidevaux, Nedjar-Arroume, & Guillochon, like antihypertensive activity, antioxidant activity or opioid activity 1999), opioid peptides (Froidevaux, Vanhoute, Lecouturier, Dhulster, & among others (Arihara & Ohata, 2010). The inhibition of the angiotensin Guillochon, 2008; Piot, Zhao, Guillochon, Ricart, & Thomas, 1992), analge- I-converting enzyme (ACE) probably constitutes the most relevant bio- sic peptides (Zhao, Molina, & Piot, 1997) and antioxidant peptides activity. This enzyme participates in the renin–angiotensin system (Chang, Wu, & Chiang, 2007). For instance, porcine hemoglobin hydro- where angiotensin I is converted into angiotensin II that constricts the lyzed with commercial proteases (alcalase followed by flavorenzyme) arteries and, as a consequence, increases the blood pressure. An effective exerted good antioxidant activities, especially ferrous ion chelating ability way to reduce blood pressure is through the inhibition of ACE (Ahmed & and DPPH radical scavenging activity being correlated to the larger molec- Mugurama, 2010). In any case, ACE inhibitory activity in vitro effects ular weight peptides fraction collected after gel filtration (Chang et al., does not mean an in vivo effect. The reason is that peptides must reach 2007). the cardiovascular system in an intact form (e.g. not being affected by di- Antioxidant and free radical scavenging peptides with in vitro and gestive human proteases and being absorbed through the intestinal wall in vivo activity were obtained through hydrolysis of pork myofibrillar into the blood). It has been reported that the bioactivity intensity is in- proteins with papain (Arihara, 2006b; Saiga, Tanabe, & Nishimura, versely correlated to the peptide length (Vermeirssen, Van Camp, & 2003). Furthermore, 3 peptides (Asp-Leu-Tyr-Ala, Ser-Leu-Tyr-Ala Verstraete, 2004). Therefore, the peptides that can inhibit ACE in vitro and Val-Trp) with an anti-fatigue effect as observed with laboratory and further exert antihypertensive effect in vivo have shown great rats could be isolated and identified (Arihara, 2006b). Protein hydro- promise in the development of a novel therapeutics and functional lyzates with molecular size below 3000 Da showed an hypocholester- food for preventing hypertension. olemic effect observed in laboratory rats probably by interfering the A number of bioactive peptides resulting from meat proteins hy- esteroid absorption (Nagaoka, 2006). drolysis have been reported in recent literature. The simulated diges- Some commercial applications of bioactive peptides in the fish in- tion of pork meat proteins with gastrointestinal proteases like pepsin, dustry have been reported (Lee, Barrow, Kim, Miyashita, & Shahidi, trypsin, chimotrypsin or pancreatin releases peptides that showed in 2011). Such applications include hydrolyzed bonito products like vitro and in vivo antihypertensive activity when assayed with sponta- PeptACE (Natural Factors), Bonito Peptide (Ortho Molecular Prod- neously hypertensive rats. In fact, some of those peptides consisting ucts), Levenorm (Ocean Nutrition Canada) and bioactive peptides of two pentapeptides from titin (Lys-Ala-Pro-Val-Ala and Pro-Thr- from fish proteins (Matís — Icelandic Food and Biotech R&D), making Pro-Val-Pro) and a tripeptide from nebulin (Arg-Pro-Arg), exerted a it a real possibility that also commercial applications from meat by- significant blood pressure decrease in the rats just after 8 h of products can be expected in the near future. 294 F. Toldrá et al. / Meat Science 92 (2012) 290–296

3.3. Protein: generation of antimicrobial peptides Proteins recovered from the animal rendering process (e.g., blood- meal, bonemeal or meat) are used to produce protein based foams. The first identification of a peptide in bovine hemoglobin with These foams are derived from hydrolyzed proteins with the objective antibacterial activity corresponded to the fragment 33–61 of the α- to obtain a product with improved physical properties (e.g., reduced chain of bovine hemoglobin (Fogac et al., 1999). Such peptide was ac- surface tension, increased foamability and foam stability) (Bressler, tive against Gram-positive bacteria and fungus isolated from the he- 2009). In other cases, hydrolyzed proteins, either chemically or enzy- molymph of a tick parasitizing the bovines (Boophilus microplus) matically, are used as flavor ingredients because they contain small (Fogac et al., 1999). Another four antimicrobial peptides active peptides and free amino acids with flavoring properties. These hydro- against Micrococcus luteus A270, Listeria innocua, Escherichia coli and lyzates may also react with reducing sugars to generate relevant Salmonella enteritidis were isolated from peptic digested bovine he- flavors. Some dipeptides (Glu-Glu and Glu-Val) and tripeptides moglobin at low degree of hydrolysis (Daoud et al., 2005; Nedjar- (Ala-Asp-Glu, Ala-Glu-Asp, Ser-Pro-Glu and Asp-Glu-Glu) having Arroume et al., 2006). Three peptides corresponded to fragments of umami taste were obtained after the hydrolysis of chicken protein the α chain of the bovine hemoglobin (α107–141, α137–141, and extracts with bromelain (Maehashi, Matsuzaki, Yamamoto, & Udaka, α133–141) and one from the β chain (β126–145). It was necessary 1999). to clarify if almost all of the hemoglobin was effectively able to exhibit antimicrobial activity or if these peptides contained a common part or 4. Feed and pet food applications structure giving the biological activity. Thus, it was reported that all active peptides derived from α 107–141 contained the necessary One of the traditional uses of raw and rendered animal by- KYR sequence for the antimicrobial activity, which is the minimal an- products has been its incorporation as ingredients in feeds and timicrobial sequence from the hemoglobin α-chain (Catiau et al., pet foods. These materials provide diets with adequate nutrients 2011). Similarly, the peptide β114–145 and its peptic derivatives con- and good digestibility (Murray,Patil,Fahey,Merchen,&Hughes, taining the RYH sequence were found as the most antimicrobial pep- 1997). In fact, meat and bone meal, blood meal, plasma meal, hy- tides, especially the RYH peptide which was the shortest one (Catiau drolyzed feather meal, tallow or grease contain protein, fat, min- et al., 2011). eralsandtraceelementsaswellasBvitaminsandsomefat- Twenty-four active peptides were located in the α chain and were soluble vitamins which are required in animal nutrition (Pearl, classified into three families: α1 derived from peptide α 1–32, α2 de- 2004). As mentioned for human food, the functions and usefulness rived from peptide α 33–98, and α3 derived from peptide α 107–141. of some organs may vary because of relevant fluctuations in the nu- Six active peptides were located in the β chain and were classified trient content depending on the animal species from which they into two families; β1 and β2 derived from β 1–30 and β 114–145 are obtained. peptides, respectively (Nedjar-Arroume et al., 2008). Different methods for recovering nutrients from animal by- The pepsin hydrolysis conditions were changed by using 40% meth- products and its use as ingredient in feeds have been reported. anol, 30% ethanol, 20% propanol or 10% butanol. The selective and re- Some examples are the separation of protein from the animal by- strictive hydrolyzate of hemoglobin contained only 29 peptides. 26 product materials and drying the meal (Alexis & Robert, 2004), the peptides showed an antibacterial activity against Micrococcus luteus, production of high-quality amino acid solution from the blood of Listeria innocua,andEscherichia coli with a minimum inhibitory concen- harvested animals through the use of specific microbial cultures tration (MIC) from 187.1 to 1 μM. Among them, 13 peptides were (Giu & Giu, 2010) or the generation of crude protein extracts from obtained under those new hydrolysis conditions (Adje et al., 2011). Fur- keratin, a fibrous structural protein that constitute structural compo- thermore, the hydrolysis of bovine hemoglobin with pig pepsin in the nent of hair, nail, feather and outer layer of skin, through enzymatic presence of 30% ethanol released several peptides that were identified hydrolysis with keratinase (Deivasigamani & Alagappan, 2008). as TKAVEHLDDLPGALSELSDLHAHKLRVDPVNFKLL SHSLL, LDDLPGAL- SELSDLHAHKLRVDPVNFKLLSHSL, KLLSHSL, and LLSHSL. They corre- 5. Other non-food, non-feed industrial applications spond respectively to the 67–106, 73–105, 99–105, and 100–105 fragments of the α chain of bovine hemoglobin. These peptides have Rendered fat has expanded its use for a variety of cosmetic appli- an antibacterial activity against Kocuria luteus A270, Listeria innocua, cations like hand and body lotions, creams and bath products. Fatty Escherichia coli,andStaphylococcus aureus with a MIC between 187.1 acids are used in a large amount of chemical processes like rubber and 35.2 μM. On the other hand, these peptides also displayed inhibito- and plastic polymerization, softeners, lubricants and plasticizers. Col- ry activity against the angiotensin converting enzyme (ACE) with an lagen, gelatin and glycerin are also used as ingredients for surfactants, IC50 range from 42.55 to 1095 μM. (Adje, Balti, Kouach, Guillochon, & paints, varnishes, adhesives, antifreeze, cleaners, polishes and phar- Nedjar-Arroume, 2011). maceuticals (Pearl, 2004). In recent years, low cost vegetable and animal fat wastes were used 3.4. Proteins: other food applications as raw materials for biodiesel production, replacing conventional diesel fuel by fatty acid methyl esters. Biodiesel can be a valid alternative to Gelatin is a water-soluble animal protein produced through the diesel fuel with non significant modifications to the vehicle engines. hydrolysis of collagen. Gelatin is rich in glycine and proline but poor Furthermore, it has several additional advantages: it is biodegradable, in tryptophan and methionine. Gelatin has good gel-forming ability non toxic and with a favorable combustion emission profile that leads that makes it of interest in the food industry for a wide variety of ap- to reductions in carbon dioxide, carbon monoxide, particulate matter plications like desserts, candies, bakery, jellied meat, ice cream and and unburned hydrocarbon (Moreira, Dias, Almeida, & Alvim-Ferraz, dairy products. Collagen is quite abundant in the carcass and can be 2010). The most common way to produce biodiesel is by transesterifica- extracted from the animal skin, bones, tendons and ossein. The ex- tion of the fats with a low molecular weight alcohol to yield a mixture of traction of gelatin follows a four stage process consisting of the selec- fatty acid methyl esters and glycerol as a side product. Raw materials tion of the collagen content in the raw material, the removal of non- consist of low cost animal fat by-products like poultry fat or tallow collagen materials, the controlled hydrolysis of collagen into gelatin and the transesterification reactions are acid, alkali or enzymatic- and finally the recovery and drying of gelatin (Ockerman & Basu, catalyzed (Bhatti, Hanif, Qasim, & Rheman, 2008; Moreira et al., 2010). 2006). Typical food industry applications of gelatin are found in bak- Other authors propose the use of supercritical transesterification to in- ery, dairy and meat products as clarifying agent, stabilizer or protec- crease biodiesel profitability for continuous flow processes and without tive coating material (Djagny, Wang, & Xu, 2001). glycerol generation as by-product (Marulanda, Anitescu, & Tavlarides, F. Toldrá et al. / Meat Science 92 (2012) 290–296 295

2010). High yields have been reported after hydrodooxygenation and Chang, C. -Y., Wu, K. -C., & Chiang, S. H. (2007). Antioxidant properties and protein com- positions of porcine haemoglobin hydrolysates. Food Chemistry, 100, 1537–1543. hydroisomerization in tubular reactors (Herskowitz, 2008). Chen, M. J., & Lin, C. W. (2002). Factors affecting the water-holding capacity of fibrino- Hides are traditionally used for conversion into leather (Ockerman & gen/plasma protein gels optimized by response surface methodology. Journal of Basu, 2004b) and it is continuing nowadays. For instance, the yield of Food Science, 67, 2579–2582. – fi Cofrades, S., Guerra, N. I. A., Carballo, J., Fernández-Martin, F., & Jiménez-Colmenero, F. cattle hide is about 7 8% of the animal's live weight and is classi ed in (2000). Plasma protein and soy fiber content effect on bologna sausage properties accordance to weight, sex, defects and skill of removal. Uses are quite as influenced by fat levels. Journal of Food Science, 65, 281–287. extended and involve shoes, handbags, purses, gloves, fancy leather Daoud, R., Dubois, V., Bors-Dodita, L., Nedjar-Arroume, N., Krier, F., Chihib, N. E., et al. clothes, belts, etc. Hides also constitute a source of collagen. (2005). New antibacterial peptide derived from bovine hemoglobin. Peptides, 26, 713–719. Deivasigamani, B., & Alagappan, K. M. (2008). Industrial application of keratinase and 6. Conclusions soluble proteins from feather keratine. Journal of Environmental Biology, 29, 933–936. Djagny, K. B., Wang, Z., & Xu, S. (2001). Gelatin: A valuable protein for food and phar- There is a large variety of applications of meat by-products. In ad- maceutical industries, review. Critical Reviews in Food Science and Nutrition, 41, dition to the usual applications like human and animal foods, ren- 481–492. Duarte, R. T., Carvalho Simoes, M. C., & Sgarbieri, V. C. (1999). Bovine blood compo- dered fat for cosmetics and chemicals and hides for leather, recent nents: Fractionation, composition, and nutritive value. Journal of Agricultural and innovative proposals include the use of proteins for better technolog- Food Chemistry, 47, 231–236. ical or nutritional properties, the generation of bioactive and antimi- EC (2001). Regulation 999/2001 of the European Parliament and of the Council of 22 crobial peptides or the use of animal fats for biodiesel production. May 2001 laying down rules for the prevention, control and eradication of certain transmissible spongiform encephalopathies. Official Journal of the European Union, Regardless of the final product's destination, it is still necessary to 147,1–69. employ the most up-to-date and effective tools to analyze by- EC (2004). Regulation 853/2004 of the European Parliament and of the Council of 29 fi products for nutritional properties, to search for key active molecules April 2004 laying down speci c hygiene rules for on the hygiene of foodstuffs. Of- ficial Journal of the European Union, 139,1–55. in food and nutrition, as well as for other non-food applications like EC (2009). Regulation 1069/2009 of the European Parliament and of the Council of 21 pharmaceuticals, cosmetics or energy, to continue innovation to- October 2009 laying down health rules as regards animal by-products and derived wards advanced value-addition of such by-products. products not intended for human consumption and repealing Regulation (EC) No 1774/2002 (Animal by-products Regulation). Official Journal of the European Union, 300,1–33. Acknowledgments Escudero, E., Toldrá, F., Sentandreu, M. A., Nishimura, H., & Arihara, K. (2012). Antihy- pertensive activity of peptides derived from the in vitro gastrointestinal digestion of pork meat. Meat Science, 91, 382–384. Grant from Vaquero Foundation for R+D on Pork Meat (Madrid, Escudero, E., Sentandreu, M. A., Arihara, K., & Toldrá, F. (2010a). Angiotensin I convert- Spain), grant AGL2010-16305 from the Spanish Ministry of Science ing enzyme inhibitory peptides generated from in vitro gastrointestinal digestion – and Innovation and FEDER funds are acknowledged. Work was pre- of pork meat. Journal of Agricultural and Food Chemistry, 58, 2895 2901. Escudero, E., Sentandreu, M. A., & Toldrá, F. (2010b). Characterization of peptides re- pared within the Unidad Asociada IAD (UPV)-IATA (CSIC) framework. leased by in vitro digestion of pork meat. Journal of Agricultural and Food Chemistry, 58, 5160–5165. FDA (2004). Interim final rule — Use of materials derived from cattle in human food References and cosmetics. Food and Drug Administration 21 CFR parts 189 and 700. 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